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Research Article Analysis of Non-Small Bowel Lesions Detected by Capsule Endoscopy in Patients with Potential Small Bowel Bleeding Fatma Ebru Akin, 1 Oyku Tayfur Yurekli, 2 Aylin Demirezer Bolat, 1 Mustafa TahtacJ, 2 Huseyin Koseoglu, 1 Eyup Selvi, 1 Naciye Semnur Buyukasik, 1 and Osman Ersoy 2 1 Ankara Ataturk Research and Teaching Hospital Gastroenterology Department, 06800 Ankara, Turkey 2 Yıldırım Beyazıt University Faculty of Medicine, Ankara Ataturk Research and Teaching Hospital Gastroenterology Department, 06800 Ankara, Turkey Correspondence should be addressed to Fatma Ebru Akin; [email protected] Received 26 February 2016; Accepted 13 March 2016 Academic Editor: Spiros D. Ladas Copyright © 2016 Fatma Ebru Akin et al. is is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Gastrointestinal (GI) bleeding cases in whom source cannot be identified aſter conventional upper and lower GI endoscopy are defined as potential small bowel bleeding. We aimed to search for lesions in the reach of conventional endoscopy in patients to whom video capsule endoscopy (VCE) had been applied for potential small bowel bleeding. 114 patients who had VCE evaluation for potential small bowel bleeding between January 2009 and August 2015 were retrospectively evaluated. Mean age of the patients was 55 ± 17 years. Female/male ratio is 39/75. In 58 patients (50.9%) bleeding lesion could be determined. Among these 58 patients 8 patients’ lesions were in the reach of conventional endoscopes. Overall these 8 patients comprised 7% of patients in whom VCE was performed for potential small bowel bleeding. Among these 8 patients 5 had colonic lesions (4 angiodysplasia, 1 ulcerated polypoid cecal lesion), 2 had gastric lesions (1 GAVE, 1 anastomotic bleeding), and 1 patient had a bleeding lesion in the duodenal bulbus. Although capsule endoscopy is usually performed for potential small bowel bleeding gastroenterologists should always keep in mind that these patients may be suffering from bleeding from non-small bowel segments and should carefully review images captured from non-small bowel areas. 1. Introduction Bleeding from the small intestine accounts for about 5–10% of all cases presenting with gastrointestinal (GI) bleeding. With recent developments of the small bowel imaging techniques like video capsule endoscopy (VCE), deep enteroscopy, and radiographic imaging, the source of bleeding in the small bowel can now be identified in the majority of these patients. e term “potential small intestinal bleeding” is proposed for patients with GI bleeding in whom normal upper and lower GI tract examinations are normal and VCE is considered. Overt small bowel bleeding refers to patients presenting with either melena or hematochezia with a bleeding source identified in the small intestine. Occult small bowel bleeding refers to patients presenting with iron deficiency anemia with or without guaiac-positive stools who are found to have a small bowel source of bleeding [1]. VCE has been recommended as a first-line procedure by recent guidelines for small bowel evaluation for GI bleeding aſter upper and lower GI sources have been excluded [1–3]. With VCE noninvasive evaluation of the small bowel has become possible, with a diagnostic yield of 38–83% in patients with suspected small bowel bleeding [4]. Furthermore, it has been shown to have superior diagnostic yield compared to small bowel follow-through [5, 6], push enteroscopy [6, 7], and computed tomography enteroclysis [8] and similar to double-balloon enteroscopy in detecting bleeding small intestinal lesions [9]. Small bowel lesions were overlooked during conventional endoscopy, either because of intermittent bleeding nature of the lesions or because some lesions are really missed. In fact there are few studies showing bleeding lesions within the reach of conventional upper endoscopy/colonoscopy that have been obviously missed during the initial examination [10–13]. Hindawi Publishing Corporation Diagnostic and erapeutic Endoscopy Volume 2016, Article ID 9063293, 5 pages http://dx.doi.org/10.1155/2016/9063293

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Research ArticleAnalysis of Non-Small Bowel Lesions Detected by CapsuleEndoscopy in Patients with Potential Small Bowel Bleeding

Fatma Ebru Akin,1 Oyku Tayfur Yurekli,2 Aylin Demirezer Bolat,1 Mustafa TahtacJ,2

Huseyin Koseoglu,1 Eyup Selvi,1 Naciye Semnur Buyukasik,1 and Osman Ersoy2

1Ankara Ataturk Research and Teaching Hospital Gastroenterology Department, 06800 Ankara, Turkey2Yıldırım Beyazıt University Faculty of Medicine, Ankara Ataturk Research and Teaching Hospital Gastroenterology Department,06800 Ankara, Turkey

Correspondence should be addressed to Fatma Ebru Akin; [email protected]

Received 26 February 2016; Accepted 13 March 2016

Academic Editor: Spiros D. Ladas

Copyright © 2016 Fatma Ebru Akin et al. This is an open access article distributed under the Creative Commons AttributionLicense, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properlycited.

Gastrointestinal (GI) bleeding cases in whom source cannot be identified after conventional upper and lower GI endoscopy aredefined as potential small bowel bleeding. We aimed to search for lesions in the reach of conventional endoscopy in patients towhom video capsule endoscopy (VCE) had been applied for potential small bowel bleeding. 114 patients who had VCE evaluationfor potential small bowel bleeding between January 2009 and August 2015 were retrospectively evaluated. Mean age of the patientswas 55 ± 17 years. Female/male ratio is 39/75. In 58 patients (50.9%) bleeding lesion could be determined. Among these 58 patients8 patients’ lesions were in the reach of conventional endoscopes. Overall these 8 patients comprised 7% of patients in whom VCEwas performed for potential small bowel bleeding. Among these 8 patients 5 had colonic lesions (4 angiodysplasia, 1 ulceratedpolypoid cecal lesion), 2 had gastric lesions (1 GAVE, 1 anastomotic bleeding), and 1 patient had a bleeding lesion in the duodenalbulbus. Although capsule endoscopy is usually performed for potential small bowel bleeding gastroenterologists should always keepin mind that these patients may be suffering from bleeding from non-small bowel segments and should carefully review imagescaptured from non-small bowel areas.

1. Introduction

Bleeding from the small intestine accounts for about 5–10%ofall cases presenting with gastrointestinal (GI) bleeding. Withrecent developments of the small bowel imaging techniqueslike video capsule endoscopy (VCE), deep enteroscopy, andradiographic imaging, the source of bleeding in the smallbowel can now be identified in the majority of these patients.The term “potential small intestinal bleeding” is proposed forpatients with GI bleeding in whom normal upper and lowerGI tract examinations are normal and VCE is considered.Overt small bowel bleeding refers to patients presentingwith either melena or hematochezia with a bleeding sourceidentified in the small intestine. Occult small bowel bleedingrefers to patients presenting with iron deficiency anemiawith or without guaiac-positive stools who are found tohave a small bowel source of bleeding [1]. VCE has been

recommended as a first-line procedure by recent guidelinesfor small bowel evaluation for GI bleeding after upper andlower GI sources have been excluded [1–3].

With VCE noninvasive evaluation of the small bowel hasbecomepossible, with a diagnostic yield of 38–83% in patientswith suspected small bowel bleeding [4]. Furthermore, ithas been shown to have superior diagnostic yield comparedto small bowel follow-through [5, 6], push enteroscopy [6,7], and computed tomography enteroclysis [8] and similarto double-balloon enteroscopy in detecting bleeding smallintestinal lesions [9].

Small bowel lesions were overlooked during conventionalendoscopy, either because of intermittent bleeding nature ofthe lesions or because some lesions are really missed. In factthere are few studies showing bleeding lesions within thereach of conventional upper endoscopy/colonoscopy that havebeen obviouslymissed during the initial examination [10–13].

Hindawi Publishing CorporationDiagnostic and erapeutic EndoscopyVolume 2016, Article ID 9063293, 5 pageshttp://dx.doi.org/10.1155/2016/9063293

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2 Diagnostic andTherapeutic Endoscopy

The aim of our study is to determine the incidence of le-sionsmissed by the preceding conventional upper endoscopyor colonoscopy.

2. Materials and Methods

We reviewed prospectively collected databases of patientsreferred to the Digestive Endoscopy Unit of the AtaturkEducation and Research Hospital in Ankara to undergo aVCE analysis between January 2009 and September 2015.117 patients were referred to our tertiary referral center forpotential small bowel bleeding. All patients had undergone atleast one upper gastrointestinal endoscopy and colonoscopybefore the VCE examination, which had failed to establish ableeding source. Indeed 65 of the 117 patients had undergonean additional endoscopy or colonoscopy (55% of the studygroup). 89 patients were evaluated at another tertiary referralcenter (mainly university hospitals) and referred to ourcenter and 28 patients were endoscopically evaluated at ourcenter. Data about patient demographics, indications for theprocedure, procedural data, and findings of the procedurewere recorded. Non-small bowel lesions were defined asbleeding lesions proximal to the papilla of Vater or distalto the ileocecal valve. Small bowel lesions were definedas bleeding lesions located between papilla of Vater andileocecal valve. Bleeding lesions were defined as lesions thatabsolutely or likely explain the cause of bleeding or anemia.

VCEwas performedwith the PillCam� capsule endoscopysystem (Given Imaging, Yokneam, Israel). Until December2014VCEwere performedbyPillCamSB2.After that date dueto renewal of the equipmentVCEwere performed by PillCamSB3.The patients were given standardized information beforethe procedure, and informed consent was obtained. Thepatients were put on low fiber diet 1 day before VCE pro-cedure. Patients fasted for 10 hours before capsule ingestion.Bowel preparation consisted of 4 liters of polyethylene glycolpreparation (Golytely�; Avicenna) or 250mL sennoside A +B calcium (XM-Diet solution�; Yenisehir Lab.). The capsulewas ingested at about 8:30 a.m. the next morning. At theend of the recording period, data recorder was removed andimages were downloaded to the computer. The recordings ofVCE were reviewed by two experienced gastroenterologists(FEA, OE). The most relevant findings obtained from VCEwere documented and categorized according to standardterminology [14] as angioectasia(s), ulcer(s), active bleedingof unknown origin, erosion(s), polyp(s)/tumor(s), incidentalabnormality of esophagus, stomach, and colon, and noabnormality.

All statistics were performed using SPSS 22 for Windows(SPSS Inc., Chicago, IL, USA).

3. Results

Capsule endoscopy was performed in 117 patients withpotential small bowel bleeding. Three patients were excludedfrom the final analyses because of the capsule retention inthe stomach. In one of these 3 patients capsule was trappedin gastric bezoar. The other patient had a history of gastricresection so capsule could not reach the small intestine. In

Table 1: Results of VCE performed for potential small bowelbleeding.

Lesions 𝑁 (114)No abnormalities 56 (49.1%)Angiodysplasia(s) 20 (17.5%)Erosion(s) 5 (4.4%)Ulcer(s) 17 (15%)Polyp/tumor 7 (6.1%)Active bleeding 7 (6.1%)Other 2 (1.8%)

the final patient reason of gastric retention could not bedetermined. Finally 114 patients were included in the study.Female/male ratio was 39/75 (34.2%/65.8%) and the meanage of the patients was 55,8 ± 17 years (range 18–88 years).VCEwas performed for occult bleeding in 36 patients (31,6%)and for overt bleeding in the rest of 78 (%68,4) patients.In 58 of 114 (50.9%) patients definite or likely cause ofthe bleeding could be identified (Table 1). Among these 58patients 8 patients’ lesions were identified as non-small bowelwithin the reach of conventional endoscopy. All of these 8patients were referred to VCE from another tertiary referralcenter (8/86, 9.3%). In none of the 28 patients who werereferred toVCE fromour center a non-small bowel lesionwaspresent causing bleeding. 8 patients with non-small bowellesions comprised 7% of all VCE procedures performed forpotential small bowel bleeding. Five of these lesions were inthe cecum, 2 were in the stomach, and 1 was in the duodenum(Table 2).Themost common lesion in these non-small bowelsources of bleeding was angiodysplasia (5/8). Four of these 8patients were actively bleeding at the time of VCE procedure.Detailed clinical information about these patients with non-small bowel source of bleeding is given below.

In a patient with occult small bowel bleeding VCErevealed gastric antral vascular ectasia (GAVE) (Figure 1(a)).Previous upper endoscopy was reported as antral gastritis.Endoscopic treatment sessions with Argon Plasma Coagula-tion (APC) were performed.

In a patient with a history of Billroth II operation forpeptic ulcer disease VCE detected active bleeding and ulceron the gastric anastomosis. Upper endoscopy performedafter VCE showed a hyperemic and fragile anastomosis line.Proton Pomp Inhibitor therapy was started.

One patient had active bleeding distal to the duodenalbulb during VCE. This patient had previously undergoneupper GI endoscopy during active bleeding and was reportedto have normal endoscopy findings. Lesion could not beidentified with VCE because of active bleeding. But a repeatendoscopy after VCE revealed an angiodysplasia at thisregion and thermocoagulation was applied.

Three patientswho applied for long lasting iron deficiencyanemia had angiodysplasia (Figure 1(b)) in the colon and 1patient had active bleeding during VCE. The colonoscopyperformed after VCE showed colonic angiodysplasia in thepatient with active bleeding from the colon. In none of thesepatients were previous colonoscopies able to define theselesions.Thermocoagulationwas applied in 3 of these patients.

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Diagnostic andTherapeutic Endoscopy 3

Table 2: Non-small bowel abnormalities in capsule endoscopy.

Patient number Lesion Age (years) Gender Clinical presentation of bleeding1 GAVE 64 F Occult2 Active bleeding from gastric resection anastomosis site and ulcer 67 M Overt3 Active bleeding in the duodenal bulb 65 M Overt4 Angiodysplasia in the cecum 76 M Overt5 Angiodysplasia in the colon 50 M Overt6 Active bleeding from the cecum 70 F Overt7 Active bleeding from the cecum and angiodysplasia 80 F Overt8 Ulcer in the cecum 41 F Occult

(a) (b)

(c) (d)

Figure 1: (a) CE and GAVE, (b) CE and angiodysplasia, (c) CE and ulcerated polypoid lesion, and (d) colonoscopy and ulcerated polypoidlesion. CE: capsule endoscopy; GAVE: gastric antral vascular ectasia.

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4 Diagnostic andTherapeutic Endoscopy

The patient who was found to have an ulcer in thececum had applied for anemia and abdominal pain andcolonoscopy findings before VCE were found to be nor-mal. VCE revealed an ulcer on a protrusion in the cecum(Figure 1(c)). Colonoscopy performed after VCE showed aprotrusion to the lumen in the cecum and an ulcer on top ofit (Figure 1(d)). Biopsy taken from that area revealed chronicactive colitis but the patient was lost to follow-up.

4. Discussion

It has been shown that 5–10% of GI system bleeding is smallintestinal in origin. In patients with gastrointestinal bleedingin whom upper and lower GI endoscopies are normal smallbowel should be considered as the site of bleeding. ACGrecommends to classify these patients under the term ofpotential small bowel bleeding [1].

The clinical management of these patients with potentialsmall bowel bleeding is controversial. VCE is a simple andnoninvasive imaging technique for the examination of smallbowel. Previous studies showed that VCE is able to showthe source of bleeding in the small intestine in patients withpotential small bowel bleeding [4, 15–20]. In patients withpotential small bowel bleeding and in whom upper andlower GI system endoscopies cannot define the source ofbleeding next step in the diagnostic algorithm is proposedto be VCE [1–3]. We were able to find definite or likelyreason of bleeding in 50.9% of patients with potential smallbowel bleeding who had undergone VCE. Interestingly in7% of our patients bleeding lesion was in the reach ofconventional upper or lower endoscopy. These patients hadundergone at least one upper and lower endoscopy beforethe VCE procedure. The reasons of missing these lesionsapparent onVCEwith conventional endoscopy are unknown.One reason might be the small lesion size. Also somelesions being on unexpected sites might have caused missingof these lesions. Furthermore nonbleeding lesions duringconventional endoscopy might have been noticed duringactive bleeding at the time of VCE examination. Half ofour 8 patients with non-small intestinal cause of bleedingduring VCE had vascular lesions. The patient who wasdiagnosed with GAVE was previously reported to have antralgastritis upon upper GI endoscopy. This patient’s previousendoscopy was performed by an experienced endoscopist.This finding is in line with results of Kitiyakara and Selby[10]. They found 3 cases of GAVE in this study. These 3patients’ endoscopies were also performed by an experiencedendoscopist and authors thought that this finding might bedue to VCE’s being performed under more physiologicalcircumstances. Angiodysplasias detected at duodenal bulb orcolon were not noticed upon previous conventional upper orlower GI endoscopy. Significant anemia or the patient beinghypotensive during examination might have caused missingof these lesions. Lack of insufflation during VCE mighthave caused these lesions to seem more prominent. Lastlyalthough these patients were referred from tertiary referralcenters the level of expertise of the previous endoscopistswas not exactly known. This may have caused the missing ofthese lesions. 4 patients had bleeding lesions in the cecum.

Colonoscopists might have misidentified cecum in thesepatients and prematurely terminated the colonoscopy orthese lesions might have been really missed because of beingbehind colonic haustrations. Furthermore incomplete bowelcleansing might have caused the missing of these lesions.Despite all of these potentially confounding factors currentguidelines do not recommend second-look upper or lowerGI endoscopies if the patient is not actively bleeding and firstexamination is optimal [1].

ACG recently proposed the term potential small bowelbleeding although the literature mainly comprised studiesusing the old terminological term obscure small bowelbleeding. There are a few studies describing non-small bowelreasons of obscure small bleeding upon VCE. Kitiyakaraand Selby found 9 (6.4%) cases of non-small bowel bleedingamong 140 patients who had undergone VCE for obscuresmall bowel bleeding. Results of this study show an apparentresemblance to our findings. 4 lesions were identified instomach while 5 lesions were identified in the cecum [10].

In the study performed in 2011 by Vlachogiannakos etal. in 11 of 317 (3.5%) patients who had undergone VCE forobscure small bowel, the bleeding lesion was found outsidethe small bowel within the reach of conventional endoscopy.This study showed that repeating the conventional endoscopyfor the second time in patients with obscure small bowelbleeding who have normal first upper and lower endoscopieswas not cost effective [12]. Besides ACG clinical guidelinerecommends VCE as first-line procedure in potential smallbowel bleeding patients after excluding upper and lowergastrointestinal lesions [1–3]. Second-look endoscopy andcolonoscopy are recommended if indicated in patients withcontinuing active bleeding.

Another study found non-small bowel causes of bleedingin 54 out of 637 patients (8.5%) who had undergone VCE forobscure small bowel bleeding [13]. These studies show thatin around 3.5–8.5% of patients with potential small bowelbleeding VCE was able to define the cause of bleeding withinthe reach of conventional endoscopy.We also found this ratioas 7% similar to previous reports.

5. Conclusion

In patients to whom small bowel VCE are applied for poten-tial small bowel bleeding we can still find lesions responsiblefor the bleeding within the reach of conventional endoscopy.For this reason gastroenterologists evaluating VCE shouldthoroughly review also the gastric and colonic images inorder to catch possible missed non-small bowel lesions. Thisapproach will lead to planning of therapeutic endoscopicprocedures which may improve patient outcomes.

Competing Interests

The authors declare that there are no competing interests.

Authors’ Contributions

All authors have read and approved the paper and takeresponsibility for it.

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Diagnostic andTherapeutic Endoscopy 5

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